Coupling of collective motions of the protein matrix to vibrations of the non-heme iron in bacterial photosynthetic reaction centers

Abstract

Non-heme iron is a conservative component of type II photosynthetic reaction centers of unknown function. We found that in the reaction center from Rba. sphaeroides it exists in two forms, high and low spin ferrous states, whereas in Rsp. rubrum mostly in a low spin state, in line with our earlier finding of its low spin state in the algal photosystem II reaction center (Burda et al., 2003). The temperature dependence of the non-heme iron displacement studied by Mössbauer spectroscopy shows that the surrounding of the high spin iron is more flexible (Debye temperature ~165K) than that of the low spin atom (~207K). Nuclear inelastic scattering measurements of the collective motions in the Rba. sphaeroides reaction center show that the density of vibrational states, originating from non-heme iron, has well-separated modes between lower (4-17meV) and higher (17-25meV) energies while in the one from Rsp. rubrum its distribution is more uniform with only little contribution of low energy (~6meV) vibrations. It is the first experimental evidence that the fluctuations of the protein matrix in type II reaction center are correlated to the spin state of non-heme iron. We propose a simple mechanism in which the spin state of non-heme iron directly determines the strength of coupling between the two quinone acceptors (Q(A) and Q(B)) and fast collective motions of protein matrix that play a crucial role in activation and regulation of the electron and proton transfer between these two quinones. We suggest that hydrogen bond network on the acceptor side of reaction center is responsible for stabilization of non-heme iron in different spin states.

Spectroscopic identification of reactive porphyrin motions

“…The total area 0.377 accounts for the NRVS feature at 345 cm −1 (area 0.33). The NRVS peak at 391 cm −1 (area 0.17) corresponds to the DFT predicted ν 50 mode doublet of E symmetry ( Fe(P)(Cl) Fe(P) 53 (E u ) 23 (E g ) 26 (E g ) waving 50 (E u ) 49 (E u ) 22 5. Correlation between the low frequency modes of Fe(P) and modes of B 1 , E, B 2 , and A 2 C 4v symmetry classes of Fe(P)(Br).…”

“…vestigate the vibrational dynamics of 57 Fe in protein active sites 9,[14][15][16][17][18][19][20][21][22] and in small molecules. 11,[23][24][25][26][27][28][29][30] Since the use of NRVS to measure low frequency vibrations is restricted only by the experimental resolution (∼10 cm −1 ), it provides an important opportunity to characterize thermally excitable reactive modes.…”

Chemical proprieties of the iron-quinone complex in mutated reaction centers of Rb. sphaeroides

“…In the case of the AA mutant, the spectrum contains component of the high spin reduced state of the iron atom and a small contribution of a component, whose hyperfine parameters are more similar to those observed usually in the case of the reduced low spin state of the heme-iron in cytochromes [4,12]. The AATyr spectrum is very different from those detected for WT and AA mutant BRCs.…”

“…The spectrum of WT BRCs is composed of a single doublet with hyperfine parameters characteristic for a high spin Fe 2+ state [4,11]. In the case of the AA mutant, the spectrum contains component of the high spin reduced state of the iron atom and a small contribution of a component, whose hyperfine parameters are more similar to those observed usually in the case of the reduced low spin state of the heme-iron in cytochromes [4,12].…”

“…sphaeroides and of Rp. rubrum [4,5] and an exclusively low spin state in photosystem II of algae PSI − mutant [6,7]. We focused on studies of the NHFe valence and spin states in BRCs isolated form a wild type (WT) and two mutants of Rb.…”